After numerous stage appearances and a stint on the daytime serial "The Edge of Night" (1961-63), Hagman moved to California and in 1964 landed roles in two films, the comedy "Ensign Pulver", a less than successful sequel to the popular "Mr. Roberts", and the political thriller "Fail Safe". He received some notice for his yeoman work as a philandering playwright in "The Group" (1966).

Hagman demonstrated a flair for slapstick and light comedy starring opposite Barbara Eden in the NBC sitcom "I Dream of Jeannie" (1965-70). The series was one of several in the mid-60s that explored the relationship between a mortal and a supernatural being. The sexual chemistry between the leads was one of the reasons for the show's popularity and foreshadowed a trend that continues in TV to this day. Once the two leads married, the appeal of the show began to diminish and it was taken off the air at the end of that season.

Several attempts at recapturing his success in television comedy failed. Hagman never seemed to find the right career-making role in features either. He directed and appeared in "Beware the Blob" (1972), a campy sequel to the 50s horror flick "The Blob". Hagman also offered acceptable but by no means dazzling support to Art Carney in "Harry and Tonto" (1974). In 1973, he surprised many by displaying his talents for singing and dancing opposite Lauren Bacall in the TV adaptation of the Broadway musical "Applause".

In 1978, Hagman returned to series television in the night-time soap opera "Dallas" (CBS, 1978-91). After a shaky start, the show caught on and came to reflect the greed and "anything goes" attitude of business and life in the 80s. Hagman and his character J.R. Ewing were a perfect fit. J.R. was a lovable villain, smarmy and sexy, and the actor obviously relished playing this slightly over-the-top role, winning two Emmy nominations in the process. As the success of the show grew, Hagman consolidated his power on the show, negotiating a high salary and other perks, including directing several episodes, and eventually assumed the title of co-executive producer. After thirteen years, "Dallas" left the air, a victim as much of the conservative shift in the country as of its appearance of finally having run its course.

Hagman's post-"Dallas" work never achieved comparable success or acclaim. His attempt at another series, "Staying Afloat" (1994), was part of a rotating mystery series that failed to capture viewers. He also directed a two-hour episode of "In the Heat of the Night" (CBS, 1994). Hagman played a small role as a composite character in Oliver Stone's biopic "Nixon' (1995). In the summer of 1995, it was announced that he was suffering from cirrhosis of the liver after years of heavy drinking. A cancerous growth was discovered and Hagman underwent transplant surgery in late August.Hagman returned to acting in 1998, playing Governor Fred Picker in "Primary Colors".